Ultrahigh resolution drug design I: Details of interactions in human aldose reductase-inhibitor complex at 0.66 Å

Proteins: Structure, Function and Genetics

Volumn 55, Issue 4, 2004, Pages 792-804

  Howard, E I ^a,h   Sanishvili, R ^b   Cachau, R E ^c   Mitschler, A ^a   Chevrier, B ^a   Barth, P ^d   Lamour, V ^a   Van Zandt, M ^e   Sibley, E ^e   Bon, C ^f   Moras, D ^a   Schneider, T R ^g   Joachimiak, A ^b   Podjarny, Alberto ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c SAIC FREDERICK INC   (United States)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e The Institute for Diabetes Discovery   (United States)

^f INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

^h Instituto de Fisica de Liquidos y Sistemas Biologicos   (Argentina)

Author keywords

Diabetes complications; Drug design; Subatomic resolution; X ray crystallography

Indexed keywords

ALDEHYDE REDUCTASE; ALDOSE REDUCTASE INHIBITOR; IDD 594; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG DESIGN; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME INHIBITOR INTERACTION; HUMAN; HYDROGEN BOND; INHIBITION KINETICS; MOLECULAR DYNAMICS; PKA; PRIORITY JOURNAL; STEREOCHEMISTRY; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

ACETATES; ALDEHYDE REDUCTASE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ELECTRONS; ENZYME INHIBITORS; HYDROGEN; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN CONFORMATION; SOLVENTS; THIOCARBAMATES;

EID: 2542571016     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20015     Document Type: Article

References (59)

1. Podjarny A, Howard E, Mitschler A, Chevrier B, Lecompte C, Guillot B, Pichon-Pesme V, Jelsch C. X-ray crystallography at subatomic resolution. Europhys News 2002;33.
2. Schmidt A, Lamzin VS. Veni, Vidi, Vici-atomic resolution unraveling the mysteries of protein function. Curr Opin Struct Biol 2002;12:698-703.
3. Jelsch C, Teeter MM, Lamzin V, et al. Accurate protein crystallography at ultra-high resolution: valence electron distribution in crambin. Proc Natl Acad Sci USA 2000;97:3171-3176.
4. Teeter MM, Roe SM, Heo NH. Atomic resolution (0.83 A) crystal structure of the hydrophobic protein crambin at 130 K. J Mol Biol 1993;230:292-311.
5. Rypniewski WR, Oestergaard P, Noerregaard-Madsen M, Dauter M, Wilson KS. Fusarium oxysporum trypsin at atomic resolution at 100 and 283 K: a study of ligand binding. Acta Crystallogr D 2001:57:8-19.
6. Kuhn P, Knapp M, Soltis M, et al. The 0.78 Å structure of a serine protease: Bacillus lentus subtilisin. Biochemistry 1998;37:13446-13452.
7. Esposito L, Vitagliano L, Mazzarella L. Recent advances in atomic resolution protein crystallogrpahy. Protein Peptide Lett 2002;9:95-105.
8. Dauter Z, Lamzin VS, Wilson KS. The benefits of atomic resolution. Curr Opin Struct Biol 1997;7:681-688.
9. Oates PJ, Mylari BL. Aldose reductase inhibitors: therapeutic implications for diabetic complications. Expert Opin Investig Drugs 1999;8:2095-2119.
10. Yabe-Nishimura C. Aldose reductase in glucose toxicity: a potential target for the prevention of diabetic complications. Pharmacol Rev 1998;50:21-33.
11. Wermuth B, Münch JDB, von Wartburg JP. Stereospecificity of hydrogen transfert of aldehyde reductase. Experientia 1979;35: 1288-1289.
12. Kubiseski TJ, Hyndman DJ, Morjana NA, et al. Studies on pig muscle aldose reductase. Kinetic mechanism and evidence for a slow conformational change upon coenzyme binding. J Biol Chem 1992;267:6510-6517.
13. Grimshaw CE, Shahbaz M, Putney CG. Mechanistic basis for nonlinear kinetics of aldehyde reduction catalyzed by aldose reductase. Biochemistry 1990;29:9947-9955.
14. Humber L. The medicinal chemistry of aldose reductase inhibitors. Prog Med Chem 1987;24:299-343.
15. Rondeau JM, Tete-Favier F, Podjarny A, et al. Novel NADPH-binding domain revealed by the crystal structure of aldose reductase. Nature 1992;355:469-472.
16. Tete-Favier F, Barth P, Mitschler A, et al. Aldose reductase from pig lens. Eur J Med Chem 1995;30S:589s-603s.
17. Urzhumtsev A, Tete-Favier F, Mitschler A, et al. A " specificity" pocket inferred from the crystal structures of the complexes of aldose reductase with the pharmaceutically important inhibitors tolrestat and sorbinil. Structure 1997;5:601-612.
18. Wilson DK, Bohren KM, Gabbay KH, et al. An unlikely sugar substrate site in the 1.65 A structure of the human aldose reductase holoenzyme implicated in diabetic complications. Science 1992;257:81-84.
19. Wilson DK, Tarle I, Petrash JM, et al. Refined 1.8 A structure of human aldose reductase complexed with the potent inhibitor zopolrestat. Proc Natl Acad Sci USA 1993;90:9847-9851.
20. Bohren KM, Grimshaw CE, Lai CJ, et al. Tyrosine-48 is the proton donor and histidine-110 directs substrate stereochemical selectivity in the reduction reaction of human aldose reductase: enzyme kinetics and crystal structure of the Y48H mutant enzyme. Biochemistry 1994;33:2021-2032.
21. Schlegel BP, Jez JM, Penning TM. Mutagenesis of 3 alpha-hydroxysteroid dehydrogenase reveals a "push-pull" mechanism for proton transfer in aldo-keto reductases. Biochemistry 1998;37: 3538-3548.
22. Schlegel BP, Ratnam K, Penning TM. Retention of NADPH-linked quinone reductase activity in an aldo-keto reductase following mutation of the catalytic tyrosine. Biochemistry 1998;37:11003-11011.
23. Tarle I, Borhani DW, Wilson DK, et al. Probing the active site of human aldose reductase. Site-directed mutagenesis of Asp-43, Tyr-48, Lys-77, and His-110. J Biol Chem 1993;268:25687-25693.
24. Lee YS, Chen Z, Kador PF. Molecular modeling studies of the binding modes of aldose reductase inhibitors at the active site of human aldose reductase. Bioorg Med Chem 1998;6:1811-1819.
25. Cachau R, Howard E, Barth P, et al. The subatomic resolution structure of human aldose reductase shows the catalytic mechanism. J Phys IV France 2000;10:3-13.
26. Singh SB, Malamas MS, Hohman TC, et al. Molecular modeling of the aldose reductase-inhibitor complex based on the X-ray crystal structure and studies with single-site-directed mutants. J Med Chem 2000;43:1062-1070.
27. Harrison DHL, Bohren KM, Petsko GA, et al. The alrestatin double-decker: binding of two inhibitor molecules to human aldose reductase reveals a new specificity determinant. Biochemistry 1997;36:16134-16140.
28. Rastelli G, Costantino L., Gamberini MC, Del Corso A, Mura U, Petrash JM, et al. Binding of 1-benzopyran-4-one derivatives to aldose reductase: a free energy perturbation study. Bioorg Med Chem 2002;10:1427-1436.
29. Miyamoto S. Recent advances in aldose reductase inhibitors: potential agents for the treatment of diabetic complications. Expert Opin Ther Patents 2002;12:621-631.
30. Costantino L, Rastelli G, Gamberini MG, Barlocco D. Pharmacological approaches to the treatment of diabetic complications. Expert Opin Ther Patents 2000;10:1245-1262.
31. Ehrig T, Bohren KM, Prendergast FG, et al. Mechanism of aldose reductase inhibition: binding of NADP+/NADPH and alrestatin-like inhibitors. Biochemistry 1994;33:7157-7165.
32. Kador PF, Lee YS, Rodriguez L, et al. Identification of an aldose reductase inhibitor site by affinity labeling. Bioorg Med Chem 1995;3:1313-1324.
33. Griffin BW, McNatt LG. Characterization of the reduction of 3-acetylpyridine adenine dinucleotide phosphate by benzyl alcohol xatalyzed by aldose reductase. Arch Biochem Biophys 1986;246: 75-81.
34. Harrison DH, Bohren KM, Ringe D, Petsko GA, Gabbay KH. An anion binding site in human aldose reductase: mechanistic implications for thebinding of citrate, cacodylate, and glucose 6-phosphate. Biochemistry 1994;33:2011-2020.
35. Liu SQ, Bhatnagar A, Srivastava SK. Does sorbinil bind to the substrate binding site of aldose reductase? Biochem Pharmacol 1992;44:2427-2429.
36. Muzet N, Guillot B, Jelsch C, et al. Electrostatic complementarity in an aldose reductase complex from ultra-high-resolution crystallography and first-principles calculations. Proc Natl Acad Sci USA 2003;100:8742-8747.
37. Chakrabarti P, Chakrabarti S. C-H... O hydrogen bond involving proline residues in alpha-helices. J Mol Biol 1998;284:867-873.
38. Petrash JM, Harter TM, Devine CS, et al. Involvement of cysteine residues in catalysis and inhibition of human aldose reductase-site-directed mutagenesis of Cys-80, Cys-298, and Cys-303. J Biol Chem 1992;267:24833-24840.
39. Podjarny AD, Howard EI, Urzhumtsev A, et al. A multicopy modeling of the water distribution in macromolecular crystals. Proteins Struct Funct 1997;28:303-312.
40. Makarov VA, Feig M, Andrews BK, et al. Diffusion of solvent around biomolecular solutes: a molecular dynamics simulation study. Biophys J 1998;75:150-158.
41. 3 groups. Acta Crystallogr 1980;B36:628-630.
42. Pflugrath J, Quiocho F. Sulphate sequestered in the sulphate-binding protein of Salmonella typhimurium is bound solely by hydrogen bonds. Nature 1985;314:257-260.
43. Cambridge crystallographic data base. Cambridge, UK: Cambridge Crystallographic Data Center; 2001.
44. Jeffrey GA, Saenger W. Hydrogen bonding in biological structures. Heidelberg: Springer-Verlag; 1991.
45. El-Kabbani O, Carper DA, McGowan MH, et al. Studies on the inhibitor-binding site of porcine aldehyde reductase: crystal structure of the holoenzyme-inhibitor ternary complex. Proteins Struct Funct Genet 1997;29:186-192.
46. El-Kabbani O, Ramsland P, Darmanin C, et al. Structure of human aldose reductase holoenzyme in complex with statil: an approach to structure-based inhibitor design of the enzyme. Proteins Struct Funct Genet 2003;50:230-238.
47. Calderone V, Chevrier B, Van Zandt M, et al. The structure of human aldose reductase bound to the inhibitor IDD384. Acta Crystallogr D 2000;D56:536-540.
48. Weik M, Ravelli RB, Kryger G, et al. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc Natl Acad Sci USA 2000;97:623-628.
49. Howard E, Lamour V, Mitschler A, et al. Resolution improvement to 0.9A in crystals of human aldose reductase. Acta Crystallogr 1999; A55(Suppl):P09.OB.001.
50. Shedlovsky T. In: The behavior of carboxylic acids in mixed solvents. Pesce B, editor. Electrolytes. New York: Pergamon Press; 1962. p 146-151.
51. Lamour V, Barth P, Rogniaux H, et al. Production of crystals of human aldose reductase with very high resolution diffraction. Acta Crystallogr D 1999;D55:721-723.
52. Westbrook EM, Naday I. Charge-coupled device-based area detectors. Methods Enzymol 1997;276:233-268.
53. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326.
54. Brunger AT, et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr 1998;D54:905-921.
55. Sheldrick GM, Schneider TR. Shelxl-high-resolution refinement. Methods Enzymol 1997;277:319-343.
56. Collaborative Computational Project N. The CCP4 suite: programs for protein crystallography. Acta Crystallogr 1994;D50:760-763.
57. Jones TA, Cowan S, Zou J-Y, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst 1991;A47:110-119.
58. DeLano WL. PyMOL: an open-source molecular graphics tool. Ccp4 Newslett Protein Crystallogr 2002;40:11.
59. Burnett MN, Johnson CK. ORTEP-III: Oak Ridge Thermal Ellipsoid Plot Program for crystal structure illustrations. Oak Ridge, TN: Oak Ridge National Laboratory; 1996.